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Ancestral reconstruction of fungal symbiosis in liverworts. The trees are mirror images of a Bayesian inference phylogeny produced using 26S, the trnK-psbA spacer, and the phylogenies of Forrest et al. (2006) and Flores et al. (2017). Ancestral reconstruction was performed using the Markov 1-parameter model. The grid indicates the presence of different Glomeromycotina and Mucoromycotina families. Family initials represent Gl, Glomeraceae; Cl, Claroideoglomeraceae; Di, Diversisporaceae; Gi, Gigasporaceae; Ac, Acaulosporaceae; UA, Undescribed Archaeosporales A; UB, Undescribed Archaeosporales B; Ar, Archaeosporaceae; Pa, Paraglomeraceae; A, Putative new Endogonales family A (Fig. 1); De, Densosporaceae; B, Putative new Endogonales family B; C, Putative new Endogonales family C; En, Endogonaceae. The gain and loss events are highlighted by green (gain) and pink (loss) arrows. See also Fig. S3. Examples of the different liverwort groups; (a) Pelliidae - Fossombronia foveolata, (b) Marchantiopsida - Asterella australis, (c) Haplomitriopsida - Treubia pygmaea. Note that the liverwort genus Preissia is now subsumed into Marchantia (Long et al. 2016)
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Like the majority of land plants, liverworts regularly form intimate symbioses with arbuscular mycorrhizal fungi (Glomeromycotina). Recent phylogenetic and physiological studies report that they also form intimate symbioses with Mucoromycotina fungi and that some of these, like those involving Glomeromycotina, represent nutritional mutualisms. To c...
Citations
... Arbuscular mycorrhizal (AM) fungi are widespread symbionts of plants, recruiting from Glomeromycotina and Mucoromycotina clades, and colonizing roots/rhizoids/thalli of a majority of plant species on Earth Rimington et al. 2019). These fungi are heavily implicated in bidirectional transfers of mineral nutrients and carbon between plants and soil, in soil aggregate stabilization, as well as in the maintenance/promotion of soil and ecosystem diversity and stability upon fluctuating/changing environmental conditions (van der Heijden et al. 2008;Bardgett and van der Putten 2014;Powell and Rillig 2018). ...
Specific biomarker molecules are increasingly being used for detection and quantification in plant and soil samples of arbuscular mycorrhizal (AM) fungi, an important and widespread microbial guild heavily implicated in transfers of nutrients and carbon between plants and soils and in the maintenance of soil physico-chemical properties. Yet, concerns have previously been raised as to the validity of a range of previously used approaches (e.g., microscopy, AM-specific fatty acids, sterols, glomalin-like molecules, ribosomal DNA sequences), justifying further research into novel biomarkers for AM fungal abundance and/or functioning. Here, we focused on complex polar lipids contained in pure biomass of Rhizophagus irregularis and in nonmycorrhizal and mycorrhizal roots of chicory (Cichorium intybus), leek (Allium porrum), and big bluestem (Andropogon gerardii). The lipids were analyzed by shotgun lipidomics using a high-resolution hybrid mass spectrometer. Size range between 1350 and 1550 Da was chosen for the detection of potential biomarkers among cardiolipins (1,3-bis(sn-3′-phosphatidyl)-sn-glycerols), a specific class of phospholipids. The analysis revealed a variety of molecular species, including cardiolipins containing one or two polyunsaturated fatty acids with 20 carbon atoms each, i.e., arachidonic and/or eicosapentaenoic acids, some of them apparently specific for the mycorrhizal samples. Although further verification using a greater variety of AM fungal species and samples from various soils/ecosystems/environmental conditions is needed, current results suggest the possibility to identify novel biochemical signatures specific for AM fungi within mycorrhizal roots. Whether they could be used for quantification of both root and soil colonization by the AM fungi merits further scrutiny.
... Mucoromycotina 'fine root endophytes' (MFRE) represents a distinct group of mycorrhizaforming fungi belonging to the Mucoromycotina that often coexist with AMF in the root systems [76]. However, unlike AMF, MFRE fungi can be cultivated and exhibit flexible trophic status [76,78]. Notably, they play a more prominent role in enhancing plant N and Pi uptake, and are likely to contribute more N assimilation to plants than do AMF [79]. ...
... Notably, they play a more prominent role in enhancing plant N and Pi uptake, and are likely to contribute more N assimilation to plants than do AMF [79]. It is intriguing to observe that the establishment of ECM associations in oak trees is primarily supported by an MFRE fungus [78]. The availability of a wide variety of cultured MFRE strains and forthcoming genomic information presents valuable opportunities to delve into the underlying mechanisms of their nutritional strategies in this emerging model. ...
Establishing mutualistic relationships between plants and fungi is crucial for overcoming nutrient deficiencies in plants. This review highlights the intricate nutrient sensing and uptake mechanisms used by plants in response to phosphate and nitrogen starvation, as well as their interactions with plant immunity. The coordination of transport systems in both host plants and fungal partners ensures efficient nutrient uptake and assimilation, contributing to the long-term maintenance of these mutualistic associations. It is also essential to understand the distinct responses of fungal partners to external nutrient levels and forms, as they significantly impact the outcomes of symbiotic interactions. Our review also highlights the importance of evolutionarily younger and newly discovered root-fungus associations, such as endophytic associations, which offer potential benefits for improving plant nutrition. Mechanistic insights into the complex dynamics of phosphorus and nitrogen sensing within diverse root-fungus associations can facilitate the identification of molecular targets for engineering symbiotic systems and developing plant phenotypes with enhanced nutrient use efficiency. Ultimately, this knowledge can inform tailored fertilizer management practices to optimize plant nutrition.
... Furthermore, the plant-associated order Endogonales remains highly undersampled despite recent advances [24,88]. Some of its "fine root endophytes" colonize early-diverging plants, and sometimes co-occur with AMF [89,90]. The average genome size in Mucoromycotina species ranges from 35 to 50 Mbp, with species of Umbelopsis at the low end of the spectrum (22)(23)(24)(25)(26)(27)(28)(29)(30) and Endogonales such as Jimgerdemannia species at the higher end (240 Mbp) (Supplementary Table S1). ...
The first genome sequenced of a eukaryotic organism was for Saccharomyces cerevisiae, as reported in 1996, but it was more than 10 years before any of the zygomycete fungi, which are the early-diverging terrestrial fungi currently placed in the phyla Mucoromycota and Zoopagomycota, were sequenced. The genome for Rhizopus delemar was completed in 2008; currently, more than 1000 zygomycete genomes have been sequenced. Genomic data from these early-diverging terrestrial fungi revealed deep phylogenetic separation of the two major clades—primarily plant—associated saprotrophic and mycorrhizal Mucoromycota versus the primarily mycoparasitic or animal-associated parasites and commensals in the Zoopagomycota. Genomic studies provide many valuable insights into how these fungi evolved in response to the challenges of living on land, including adaptations to sensing light and gravity, development of hyphal growth, and co-existence with the first terrestrial plants. Genome sequence data have facilitated studies of genome architecture, including a history of genome duplications and horizontal gene transfer events, distribution and organization of mating type loci, rDNA genes and transposable elements, methylation processes, and genes useful for various industrial applications. Pathogenicity genes and specialized secondary metabolites have also been detected in soil saprobes and pathogenic fungi. Novel endosymbiotic bacteria and viruses have been discovered during several zygomycete genome projects. Overall, genomic information has helped to resolve a plethora of research questions, from the placement of zygomycetes on the evolutionary tree of life and in natural ecosystems, to the applied biotechnological and medical questions.
... Despite these various advances, mechanisms leading to the mycorrhizal transition, and more generally the evolution of mycorrhizas, are far from understanding. Taking a leap forward with this notion, Leho Tedersoo (Tartu University, Estonia) proposed a focus on the Endogonomycetes lineage, which experienced multiple independent shifts to the EM fungal lifestyle, thus offering a promising playground to investigate mycorrhizal evolution (Chang et al., 2019;Rimington et al., 2019). Noteworthy, Mark Brundrett (University of Western Australia, Australia) raised one of the challenges of in silico analyses that include root and mycorrhizal coevolution studies: database reliability. ...
... Finally, associated with rooting structures is yet another key innovation of embryophytes-the ability to form mycorrhizal associations (Fig. 5m) to facilitate the uptake of soil minerals 47,71,217 . That mycorrhizal associations are formed by extant liverwort gametophytes 74,[218][219][220] and both generations of Rhynie Chert species 147,148,221 indicates that the ancestral embryophyte gametophyte formed mycorrhizal associations, and that such associations were later co-opted during the sporophyte generation in tracheophytes. Communication between the ancestral embryophyte and mycorrhizal fungi may have been in part mediated by a secreted strigolactone, bryosymbiol, whose biosynthesis is broadly conserved across land plants and is induced under phosphate-limiting conditions in the extant liverwort Marchantia paleacea 73 . ...
The origin of a land flora fundamentally shifted the course of evolution of life on earth, facilitating terrestrialization of other eukaryotic lineages and altering the planet’s geology, from changing atmospheric and hydrological cycles to transforming continental erosion processes. Despite algal lineages inhabiting the terrestrial environment for a considerable preceding period, they failed to evolve complex multicellularity necessary to conquer the land. About 470 million years ago, one lineage of charophycean alga evolved complex multicellularity via developmental innovations in both haploid and diploid generations and became land plants (embryophytes), which rapidly diversified to dominate most terrestrial habitats. Genome sequences have provided unprecedented insights into the genetic and genomic bases for embryophyte origins, with some embryophyte-specific genes being associated with the evolution of key developmental or physiological attributes, such as meristems, rhizoids and the ability to form mycorrhizal associations. However, based on the fossil record, the evolution of the defining feature of embryophytes, the embryo, and consequently the sporangium that provided a reproductive advantage, may have been most critical in their rise to dominance. The long timeframe and singularity of a land flora were perhaps due to the stepwise assembly of a large constellation of genetic innovations required to conquer the terrestrial environment. This Review summarizes our current knowledge from genomics and fossil records about the evolutionary transition from charophycean algae to embryophytes, with a focus on the progressive assembly of the embryophyte genetic innovations during terrestrialization.
... Other plant-fungus networks, especially those comprising Mucoromycotina or Cantharellales, tend to have less connected, un-nested, and even modular structures, reflecting the higher specificity of these plant-fungus interactions. Our results thus support the idea that non-Glomeromycotina plant-fungus networks tend to have un-nested structures, as previously observed in local communities of angiosperms [43,94] or in the liverwort-Mucoromycotina network on a global scale [95]. By separately looking at the main fungal lineages, our approach thus better captured the peculiar patterns of interactions with plants of these different fungal lineages, which can be missed when merging and studying all fungi in the same framework [42]. ...
Background
The root mycobiome plays a fundamental role in plant nutrition and protection against biotic and abiotic stresses. In temperate forests or meadows dominated by angiosperms, the numerous fungi involved in root symbioses are often shared between neighboring plants, thus forming complex plant-fungus interaction networks of weak specialization. Whether this weak specialization also holds in rich tropical communities with more phylogenetically diverse sets of plant lineages remains unknown. We collected roots of 30 plant species in semi-natural tropical communities including angiosperms, ferns, and lycophytes, in three different habitat types on La Réunion island: a recent lava flow, a wet thicket, and an ericoid shrubland. We identified root-inhabiting fungi by sequencing both the 18S rRNA and the ITS2 variable regions. We assessed the diversity of mycorrhizal fungal taxa according to plant species and lineages, as well as the structure and specialization of the resulting plant-fungus networks.
Results
The 18S and ITS2 datasets are highly complementary at revealing the root mycobiota. According to 18S, Glomeromycotina colonize all plant groups in all habitats forming the least specialized interactions, resulting in nested network structures, while Mucoromycotina ( Endogonales ) are more abundant in the wetland and show higher specialization and modularity compared to the former. According to ITS2, mycorrhizal fungi of Ericaceae and Orchidaceae , namely Helotiales , Sebacinales , and Cantharellales , also colonize the roots of most plant lineages, confirming that they are frequent endophytes. While Helotiales and Sebacinales present intermediate levels of specialization, Cantharellales are more specialized and more sporadic in their interactions with plants, resulting in highly modular networks.
Conclusions
This study of the root mycobiome in tropical environments reinforces the idea that mycorrhizal fungal taxa are locally shared between co-occurring plants, including phylogenetically distant plants (e.g. lycophytes and angiosperms), where they may form functional mycorrhizae or establish endophytic colonization. Yet, we demonstrate that, irrespectively of the environmental variations, the level of specialization significantly varies according to the fungal lineages, probably reflecting the different evolutionary origins of these plant-fungus symbioses. Frequent fungal sharing between plants questions the roles of the different fungi in community functioning and highlights the importance of considering networks of interactions rather than isolated hosts.
... Indeed, many Endogonales have retained saprophytic abilities (Chang et al., 2019). Therefore, the absence of specific mycorrhizal OTUs could partially explain why spores often did not F I G U R E 5 Gametophytes and sporophytes of Lycopodiaceae associate with a specific clade of Densosporaceae: Maximum-likelihood phylogenetic tree of the Endogonales (Mucoromycotina) including the 18S rRNA OTUs detected in this study, as well as reference Endogonales sequences from previous studies looking at Endogonales colonization in lycopods or other early-diverging plant lineages (Hoysted et al., 2021;Perez-Lamarque, Petrolli, et al., 2022;Rimington et al., 2015Rimington et al., , 2019. The origin of each sample is indicated in brackets, with the indication of the type of samples (lycopod gametophytes, lycopod spores, roots of lycopod sporophytes, or roots of herbaceous plants surrounding the gametophytes) where each Endogonales OTU was observed. ...
... The origin of each sample is indicated in brackets, with the indication of the type of samples (lycopod gametophytes, lycopod spores, roots of lycopod sporophytes, or roots of herbaceous plants surrounding the gametophytes) where each Endogonales OTU was observed. The taxonomy of Endogonales, including the families Endogonaceae, Densosporaceae, and the families 'A'', 'B'', and 'C'', follows the designation of Rimington et al. (2019). This phylogeny matches the Endogonales multigene phylogeny obtained by Desirò et al. (2017). ...
... Our results therefore tend to confirm the pervasiveness and importance of Mucoromycotina in lycopods (Hoysted et al., 2019;Perez-Lamarque, Petrolli, et al., 2022;Rimington et al., 2015), as in many other vascular or non-vascular plant lineages (Desirò et al., 2013;Hoysted et al., 2018;Rimington et al., 2019;Sinanaj et al., 2021). Finding frequent associations with Mucoromycotina (and infrequent associations with Glomeromycotina) in the heathland of the Hochfeld reserve, which is likely deprived of nitrogen, may be explained by the important contribution of Mucoromycotina to plant nitrogen nutrition (Howard et al., 2022;Hoysted et al., 2019). ...
Lycopodiaceae species form an early‐diverging plant family, characterized by achlorophyllous and subterranean gametophytes that rely on mycorrhizal fungi for their nutrition. Lycopodiaceae often emerge after a disturbance, like in the Hochfeld reserve (Alsace, France) where seven lycopod species appeared on new ski trails following a forest cut. Here, to better understand their ecological dynamic, we conducted a germination experiment of lycopod spores following an anthropogenic disturbance and examined their associated fungi. Only 12% of the samples germinated, and all gametophytes were abundantly colonized by a specific clade of Densosporaceae (Endogonales, Mucoromycotina), which were also present in the roots of lycopod sporophytes, but absent from the ungerminated spores and the roots of surrounding herbaceous plants, suggesting high mycorrhizal specificity in Lycopodiaceae. In addition, ungerminated spores were profusely parasitized by chytrid fungi, also present in the surrounding lycopod gametophytes and sporophytes, which might explain the low spore germination rate. Altogether, the requirement of specific mycorrhizal Mucoromycotina fungi and the high prevalence of parasites may explain why Lycopodiaceae are often rare pioneer species in temperate regions, limited to the first stages of ecological succession. This illustrates the primordial roles that belowground microbes play in aboveground plant dynamics.
... Amplification of the fungal 18S rDNA region, PCR product cloning, re-amplification of Escherichia coli colonies and DNA sequencing were carried out following Rimington et al. (2019) with 8-12 E. coli colonies re-amplified per sample. Sequences (ca. ...
... The representative sequence of each Glomeromycota OTU was queried against the AMF fungal DNA database MaarjAM (Opik et al., 2010) and named according to the best scoring hit. Representative sequences of each OTU, defined by the UCLUST algorithm, were aligned with Endogonales DNA sequences from Bidartondo et al. Rimington et al. (2019) and Endogonales sequences from GenBank, using MAFFT v 7.017 (Katoh et al., 2002) on Geneious v. 8.1.9 (Kearse et al., 2012) and used for phylogenetic analysis. ...
Fine root endophyte mycorrhizal fungi in the Endogonales (Mucoromycota arbuscular mycorrhizal fungi, M‐AMF) are now recognized as at least as important globally as Glomeromycota AMF (G‐AMF), yet little is known about the environmental factors which influence M‐AMF diversity and colonization, partly because they typically only co‐colonize plants with G‐AMF. Wild populations of Lycopodiella inundata predominantly form mycorrhizas with M‐AMF and therefore allow focussed study of M‐AMF environmental drivers. Using microscopic examination and DNA sequencing we measured M‐AMF colonization and diversity over three consecutive seasons and modelled interactions between these response variables and environmental data. Significant relationships were found between M‐AMF colonization and soil S, P, C:N ratio, electrical conductivity, and the previously overlooked micronutrient Mn. Estimated N deposition was negatively related to M‐AMF colonization. Thirty‐nine Endogonales Operational Taxonomic Units (OTUs) were identified in L. inundata roots, a greater diversity than previously recognized in this plant. Endogonales OTU richness correlated negatively with soil C:N while community composition was mostly influenced by soil P. This study provides first evidence that M‐AMF have distinct ecological preferences in response to edaphic variables also related to air pollution. Future studies require site‐level atmospheric pollution monitoring to guide critical load policy for mycorrhizal fungi in heathlands and grasslands.
... Mucoromycotina 'fine root endophytes' (MFRE), referred to previously as Glomus tenue (Greenall) or more recently Planticonsortium tenue (Walker et al., 2018), are a globally distributed group of soil fungi (Orchard et al., 2017a) that form endosymbioses with plants from across most of the land plant phylogeny (Hoysted et al., 2018Rimington et al., 2019). Despite much progress having been made in characterizing plant-MFRE symbioses in the last decade, significant challenges remain. ...
Mucoromycotina ‘Fine Root Endophytes’ (MFRE), referred to previously as Glomus tenue (Greenall) or more recently Planticonsortium tenue (Walker et al., 2018), are a globally distributed group of soil fungi (Orchard et al., 2017a) that form endosymbioses with plants from across most of the land plant phylogeny (Rimington et al., 2019; Hoysted et al., 2018; 2019). Despite much progress having been made in characterising plant‐MFRE symbioses in the last decade, significant challenges remain.
... To the best of our knowledge, there are no reports in the literature of mycothalli from north of the Arctic Circle, with the northernmost record of the symbiosis apparently being in the simple thalloid I liverwort species Fossombronia incurva and F. wondraczekii on western Iceland at 64 °N (Rimington et al. 2019). Here, in order to determine whether or not mycothalli are present in the Arctic, we report a survey for the symbiosis in leafy liverworts on west Spitsbergen. ...
Mycothalli, symbioses between liverworts and soil fungi, have not previously been recorded in the Arctic. Here, 13 species of leafy liverwort from west Spitsbergen in the High Arctic are examined for the symbiosis using epifluorescence microscopy and sequencing of fungal ribosomal (r)RNA genes amplified from plant tissues. Microscopy showed that intracellular hyphal coils, key indicators of the symbiosis, were frequent (>40% stem length colonized) in nine species of liverwort in the families Anastrophyllaceae, Lophoziaceae, Cephaloziellaceae, Cephaloziaceae and Scapaniaceae, with hyphae occurring frequently (>40% cells occupied) in the rhizoids of 10 species in the same families. Dark septate hyphae, apparently formed by ascomycetes, were frequent on the stems of members of the Anastrophyllaceae, Cephaloziellaceae and Cephaloziaceae, and typically those growing on acidic mine tailings. Sequencing of fungal rRNA genes showed the presence of nine distinct groups (based on a 3% cut-off for ITS sequence divergence) of the basidiomycete Serendipita in the Anastrophyllaceae and Lophoziaceae, with ordinations and correlative analyses showing the presence of the genus to be positively associated with the frequency of hyphal coils, the occurrence of which was positively associated with edaphic factors (soil δ15N value and concentrations of moisture, nitrogen, carbon and organic matter). We propose that the frequency of mycothalli in leafy liverworts on west Spitsbergen, which is an order of magnitude higher than at lower latitudes, may arise from benefits conferred by mycobionts on their hosts in the harsh environment of the High Arctic.
